Cytosine methylation is an ancient epigenetic modification yet its function and extent within genomes is highly variable across eukaryotes. In mammals, methylation controls transposable elements and regulates the promoters of genes. In insects, DNA methylation is generally restricted to a small subset of transcribed genes, with both intergenic regions and transposable elements (TEs) depleted of methylation. The evolutionary origin and the function of these methylation patterns are poorly understood. Here we characterise the evolution of DNA methylation across the arthropod phylum. While the common ancestor of the arthropods had low levels of TE methylation and did not methylate promoters, both of these functions have evolved independently in centipedes and mealybugs. In contrast, methylation of the exons of a subset of transcribed genes is ancestral and widely conserved across the phylum, but has been lost in specific lineages. A similar set of genes is methylated in all species that retained exon-enriched methylation. We show that these genes have characteristic patterns of expression correlating to broad transcription initiation sites and well-positioned nucleosomes, providing new insights into potential mechanisms driving methylation patterns over hundreds of millions of years.

胞嘧啶甲基化是一种古老的表观遗传修饰，但其在基因组内的功能和程度在真核生物中存在很大差异。在哺乳动物中，甲基化控制转座元件并调节基因的启动子。在昆虫中，DNA 甲基化通常仅限于一小部分转录基因，基因间区域和转座元件 (TE) 均缺乏甲基化。人们对这些甲基化模式的进化起源和功能知之甚少。在这里，我们描述了节肢动物门 DNA 甲基化的进化。虽然节肢动物的共同祖先具有低水平的 TE 甲基化并且没有甲基化启动子，但这两种功能在蜈蚣和粉蚧中都是独立进化的。相比之下，转录基因子集的外显子甲基化是祖先的，并且在整个门中广泛保守，但在特定谱系中已经丢失。在所有保留外显子富集甲基化的物种中，一组相似的基因被甲基化。我们证明这些基因具有与广泛的转录起始位点和位置良好的核小体相关的特征性表达模式，为数亿年来驱动甲基化模式的潜在机制提供了新的见解。